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Entamoeba Mitosomes Play an Important Role in Encystation by Association with Cholesteryl Sulfate Synthesis

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Entamoeba Mitosomes Play an Important Role in Encystation by Association with Cholesteryl Sulfate Synthesis Entamoeba mitosomes play an important role in encystation by association with cholesteryl sulfate synthesis Fumika Mi-ichia,1, Tomofumi Miyamotob, Shouko Takaoa, Ghulam Jeelanic, Tetsuo Hashimotod,e, Hiromitsu Haraa, Tomoyoshi Nozakic,d,1, and Hiroki Yoshidaa aDivision of Molecular and Cellular Immunoscience, Department of Biomolecular Sciences, Faculty of Medicine, Saga University, Saga, Saga 849-8501, Japan; bDepartment of Natural Products Chemistry, Graduate School of Pharmaceutical Sciences, Kyushu University, Higashi-ku, Fukuoka 812-8582, Japan; cDepartment of Parasitology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo 162-8640, Japan; dGraduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan; and eCentre for Computational Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved April 28, 2015 (received for review December 11, 2014) Hydrogenosomes and mitosomes are mitochondrion-related or- as the tricarboxylic acid (TCA) cycle, electron transport, oxida- ganelles (MROs) that have highly reduced and divergent functions tive phosphorylation, and β-oxidation of fatty acids (1, 2). Fur- in anaerobic/microaerophilic eukaryotes. Entamoeba histolytica,a thermore, unique features of mitosomes, unlike other MROs, have microaerophilic, parasitic amoebozoan species, which causes intes- not been linked to distinct roles in organisms. tinal and extraintestinal amoebiasis in humans, possesses mito- Mitosomes have been described exclusively in protistan para- somes, the existence and biological functions of which have sites including Entamoeba histolytica, the causative agent for in- been a longstanding enigma in the evolution of mitochondria. testinal and extraintestinal amoebiasis in humans. The infectious We previously demonstrated that sulfate activation, which is not diseases caused by this parasite are a serious public health generally compartmentalized to mitochondria, is a major function problem (6), and thus developing novel therapeutics to prevent of E. histolytica mitosomes. However, because the final metabo- these diseases is of great importance. We have shown that sulfate lites of sulfate activation remain unknown, the overall scheme of activation is a major metabolic pathway in E. histolytica mito- this metabolism and the role of mitosomes in Entamoeba have not somes (1, 5). Because in eukaryotes sulfate activation generally been elucidated. In this study we purified and identified choles- occurs in the cytoplasm or plastids (1, 7), its compartmentali- teryl sulfate (CS) as a final metabolite of sulfate activation. We zation to mitosomes is unprecedented. MROs are present in a then identified the gene encoding the cholesteryl sulfotransferase variety of unicellular eukaryotic organisms (2, 4); however, the responsible for synthesizing CS. Addition of CS to culture media relationship of sulfate activation to MROs is not clear. In increased the number of cysts, the dormant form that differenti- Mastigamoeba balamuthi, a microaerophilic, free-living amoeba, ates from proliferative trophozoites. Conversely, chlorate, a selec- which is a close relative of E. histolytica, the enzymes involved in tive inhibitor of the first enzyme in the sulfate-activation pathway, the sulfate-activation pathway are encoded in the genome, and inhibited cyst formation in a dose-dependent manner. These re- these proteins possess mitochondrial targeting signals; two of sults indicate that CS plays an important role in differentiation, an these enzymes are localized in MROs (8). Although other an- essential process for the transmission of Entamoeba between aerobic/microaerophilic, parasitic organisms, such as Trichomo- hosts. Furthermore, we show that Mastigamoeba balamuthi, an nas vaginalis, Giardia intestinalis, and Cryptosporidium parvum, anaerobic, free-living amoebozoan species, which is a close rela- tive of E. histolytica, also has the sulfate-activation pathway in Significance MROs but does not possess the capacity for CS production. Hence, we propose that a unique function of MROs in Entamoeba con- Evolution and diversification of organelles is a central topic in tributes to its adaptation to its parasitic life cycle. biology. Mitochondrion-related organelles (MROs) are highly modified forms of mitochondria found in anaerobic eukary- mitochondrion-related organelles | protist | sulfolipids | differentiation otes. MROs show a spectrum of functions that are either re- duced or modified from those of canonical mitochondria by itochondrion-related organelles (MROs) are derived from environmental constraints and evolutionary selection. Hence, Mcanonical mitochondria and are found in a wide range of elucidation of MRO functions will improve our understanding anaerobic/microaerophilic eukaryotes (1, 2). During the course of organelle evolution and the speciation of eukaryotes. Here, of evolution MROs have undergone secondary loss of mito- we substantiate a role of the Entamoeba mitosome, a type of chondrial functions; this loss has occurred independently multi- MRO, by showing that cholesteryl sulfate synthesized through ple times, resulting in the broad phylogenetic distribution of a mitosomal pathway regulates differentiation that is essential organisms possessing MROs (2). Furthermore, MROs occa- for the parasite’s life cycle. These findings support the contri- sionally acquire novel functions from other organisms by lateral bution of an endosymbiont-derived organelle to parasitism, gene transfer (LGT) (1, 3). Hence, MROs are not simply rem- a previously unrecognized concept that casts new light on nants of mitochondria but rather are organelles that display a organelle evolution. variety of unique features (1–5). Unique features have been demonstrated in different types of Author contributions: F.M. designed research; F.M., T.M., S.T., G.J., and T.H. performed MRO (2–4). Some anaerobic lineages of eukaryotes possess research; F.M., H.H., T.N., and H.Y. analyzed data; and F.M., T.N., and H.Y. wrote MROs (hydrogenosomes or hydrogen-producing mitochondria) the paper. that have remodeled their mitochondria drastically to couple The authors declare no conflict of interest. ATP generation with hydrogen production (2–4). Mitosomes, This article is a PNAS Direct Submission. 1To whom correspondence may be addressed. Email: [email protected] or nozaki@ another type of MRO maintained in some organisms that inhabit nih.go.jp. anaerobic/microaerophilic environments, do not produce ATP This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. or hydrogen and have lost typical mitochondrial functions, such 1073/pnas.1423718112/-/DCSupplemental. E2884–E2890 | PNAS | Published online May 18, 2015 www.pnas.org/cgi/doi/10.1073/pnas.1423718112 Downloaded by guest on October 1, 2021 possess MROs, the genomes of these organisms apparently lack We attempted to identify the gene responsible for producing PNAS PLUS genes involved in the sulfate-activation pathway (1). Moreover, CS in E. histolytica through a gene knockdown approach. Each of phylogenetic analyses revealed that E. histolytica and M. bala- the 10 SULT genes was knocked down in separate E. histolytica muthi appear to have acquired the enzymes in the sulfate-acti- transformants by antisense small RNA-mediated transcriptional vation pathway from distinct prokaryotic and eukaryotic lineages gene silencing (5, 13), and these transformants were designated by LGT (1, 8). Therefore sulfate activation is not a conserved “SULT1–10gs.” Quantitative RT-PCR (qRT-PCR) verified a function of MROs but may be a unique feature of MROs main- 92.8–99.9% reduction of the steady-state transcript level of each tained by the Entamoeba and Mastigamoeba lineages (5). target gene (Fig. S4). As expected, in SULT2–4gs, SULT6gs, and Sulfate activation is achieved by sequential reactions mediated SUTL8–10gs, only the target genes were knocked down. How- by ATP sulfurylase (AS) and adenosine 5′-phosphosulfate kinase ever, in SULT1gs, SULT5gs, and SUTL7gs, not only the target (APSK) to produce 3′-phosphoadenosine 5′-phosphosulfate genes but also two other genes (SULT5 and -7 in SULT1gs; (PAPS) (7). PAPS then acts as an activated sulfur donor to SULT1 and -7 in SULT5gs; and SULT1 and -5 in SULT7gs) were synthesize various sulfated metabolites through sulfotransferase knocked down simultaneously, probably because of high sequence (SULT) reactions. The metabolites thus produced have impor- identity (70.0–77.9%) among the regions used for gene si- tant roles in a variety of cellular events (9). In E. histolytica,we lencing in SULT1,-5,and-7. previously demonstrated that a major fraction of sulfated me- We then analyzed the profile of sulfolipids produced in tabolites are sulfolipids (1, 5). However, these sulfolipids were SULT1–10gs and control mock transformants (wild-type strain not identified, and thus the overall scheme of this metabolism in transfected with an empty vector) by metabolic labeling. Among Entamoeba remained unknown. More importantly, the role of the 10 transformants analyzed, only SULT6gs showed a differ- Entamoeba mitosomes remained an enigma. In this study, to ence in the profile of sulfolipids produced, i.e., a significant re- address these issues, we identified a sulfolipid synthesized in duction only of CS (Fig. 1). This result indicated that SULT6 E. histolytica and the gene responsible for producing it. We then encodes
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